Relationship between stiffness, internal cell pressure and shape of outer hair cells isolated from the guinea-pig hearing organ

Relationship between stiffness, internal cell pressure

and shape of outer hair cells isolated

from the guinea-pig hearing organ

E . C H A N 1 and M . U L F E N D A H L 1,2

1 Department of Physiology and Pharmacology, Karolinska Institutet

2 King Gustaf V Research Institute, Karolinska Institutet, Sweden

ABSTRACT

The mechanical properties of outer hair cells are of importance for normal hearing, and it has been

shown that damage of the cells can lead to a reduction in the hearing sensitivity. In this study, we

measured the stiffness of isolated outer hair cells in hyper- and hypotonic conditions, and examined

the change in stiffness in relation to the corresponding changes in internal cell pressure and cell shape.

The results showed that the axial stiffness of isolated outer hair cells (30±90 lm in length, 8±12 lm in

diameter), ranging from 0.13±5.39 mN m)1, was inversely related to cell length. Exposure to

hyper- and hypotonic external media with a small percentage change in osmolality caused a similar

magnitude of change in cell length and cell diameter, but an average 60% change in cell stiffness.

Therefore, a moderate osmotic change in the external medium can lead to a signi®cant alteration in cell

stiffness. The ®ndings thus indicate an important contribution of internal cell pressure to cell stiffness.

Keywords cochlea, hearing, mechanical, outer hair cell, pressure, shape, stiffness.

Received 26 March 1997, accepted 23 June 1997

The organ of Corti of the inner ear plays a signi®cant

role in the analysis of the frequencies and amplitudes of

sound. The auditory sensory cells, the outer and inner

hair cells, act as mechano-electrical transducers in the

organ by converting the mechanical vibrations of the

basilar membrane to electrical signals in the auditory

nerve. An additional feature of the outer hair cells is

that, within the hearing organ, they appear to be

capable of generating an active, mechanically tuned

response to sound stimuli (Brundin et al. 1992). This

correlates with the suggestion that the tuning charac-

teristics of the basilar membrane are dependent upon

the viability of the outer hair cells (Khanna & Leonard

1986) and that damage to the outer hair cells causes a

reduction in the hearing sensitivity of the cochlea

(Kiang et al. 1970, Dallos et al. 1972, Liberman & Kiang

1978, Kiang et al. 1986). It has also been demonstrated

that overstimulation-induced damage to the outer hair

cells is accompanied by changes in the tuning charac-

teristics of the hearing organ, indicating a reduction in

its overall stiffness (Ulfendahl et al. 1993). Moreover, it

has recently been shown that noise exposure caused a

signi®cant reduction in the stiffness of the hair cell

body (Chan et al. 1997). Isolated outer hair cells are

capable of showing a motile response to acoustic

stimulation (Canlon et al. 1988, Brundin et al. 1989,

Brundin & Russell 1994), and it was observed that the

response was reduced when a loss of stiffness occurred

in the outer hair cells (Brundin & Russell 1994). Thus,

as the various evidence implies, the mechanical prop-

erties of the outer hair cells are of great importance to

the normal sensitivity of the hearing organ.

The way in which individual outer hair cells are capable

of maintaining their cell shape following isolation from

the hearing organ has indicated an intrinsic stiffness of

the cells. The shape of the outer hair cells has been

suggested to be maintained by a ¯uid-®lled core with

positive internal cell pressure (Chertoff & Brownell

1994) and the actin ®laments along the lateral wall of

the cell (Bannister et al. 1988, Lim et al. 1989, Holley &

Ashmore 1990).

The aim of the present study was to measure the axial

stiffness of isolated outer hair cells and to obtain a

quantitative representation of the mechanical properties

of the cells. In addition, by modifying the tonicity of the

external medium, we examined the relationship be-

Correspondence: Dr Mats Ulfendahl, King Gustaf V Research Institute, Karolinska Hospital, S-171 76 Stockholm, Sweden.

Acta Physiol Scand 1997, 161, 533±539

Ó 1997 Scandinavian Physiological Society 533

tween the changes in internal cell pressure, cell shape

and axial stiffness of the outer hair cells.

MATERIALS AND METHODS

Preparation of isolated outer hair cells

Pigmented guinea-pigs (200±400 g body wt) were de-

capitated and the temporal bones were rapidly excised.

After opening the bullae, the cochleae were dissected

free and placed in tissue culture medium (Minimum

Essential Medium, with Hanks' salts, 25 mM HEPES

buffer, without L-glutamine; Gibco). The organ of Corti

was carefully detached from the basilar membrane with

a micro-scalpel. Coils of the organ were treated with

collagenase (0.5 mg mL)1) for 3 min and were rinsed at

least three times with normal culture medium. Outer

hair cells were dissociated by trituration and were al-

lowed to settle on a Cell-Tak (Becton Dickinson Lab-

ware; 1:4 diluted in 0.1 M NaHCO3) coated glass slide.

Experiments were conducted at room temperature. The

osmolality of the external medium was maintained by

constantly adding distilled water, or in later experiments

by continuous perfusion of the experimental chamber.

Microscopy and cell visualization

Glass slides containing the preparation were mounted

on an upright microscope (Zeiss ACM) equipped with a

CCD camera (Hamamatsu). The cells were viewed at

40 ´ magni®cation with a water-immersion objective

lens (NA 0.75). Images were displayed on a computer

monitor at a magni®cation of up to 5 ´ 104 times and

were recorded with an sVHS video tape recorder

(Panasonic).

Stiffness measurements

Quartz ®bres with diameters ranging from 2 to 3.5 lm

were trimmed to a length of about 1 mm, and indi-

vidual ®bres were glued to the blunt tip of a glass

pipette. Quartz ®bres used in later experiments were

coated with a thin layer of a hydrophobic, silane

compound (hexamethyldisilane, Sigma). The coating

layer was made by exposing the ®bres to a vaporized

form of the compound at 180 °C for 10 min. The

addition of silane has proved to be very effective in

preventing adherence between the ®bre and the cell

during stiffness measurements. The bending stiffness of

each quartz ®bre was calibrated using glass microbeads

(30±50 lm in diameter; Polysciences) (Howard &

Hudspeth 1988). As illustrated in Figure 1(a), a bead

was attached to the tip of a quartz ®bre causing a

displacement (d ) of the ®bre. The force (F ) exerted by

the weight of the bead could be calculated using the

equation F � 4=3pr 3 � q� G , where r is the radius of

the bead, q is the density of soda lime glass, which is

2.48 g cm)3 (Polysciences), and G is the acceleration

due to gravity, which is 9.8 m s)2. The quartz ®bre was

viewed at 25 ´ magni®cation with a modi®ed micro-

scope (Leitz) placed horizontally in a closed Perspex

cage and images were displayed on a computer monitor

via a CCD camera (Ikegami). Measurement of the ®bre

displacement was made using a frame grabber (Matrox

Magic) and image analysis software (Image Pro Plus). A

linear relationship was obtained when force (F ) was

plotted against the displacement (d ) of the ®bre, and

the bending stiffness (d) was the slope of the linear

regression line. As an example shown in Figure 1(a), a

quartz ®bre of 2.78 lm diameter and 1.24 mm length

was measured to have a bending stiffness of

0.25 mN m)1, which is, within experimental error,

comparable to the theoretical bending stiffness (Fearn

et al. 1993) of 0.32 mN m)1.

Quartz ®bres with known bending stiffness were used

to measure the axial stiffness of isolated outer hair cells.

Healthy-looking cells that were visibly birefringent,

showed no signs of swelling, shrinking or dislocation of

the nuclei, and had the upper half or more of the cell

body free from adherence to the glass slide were chosen

for stiffness measurements. The apical pole of a cell

was compressed with a quartz ®bre (Fig. 1b) and the

amount of bending of the ®bre in turn indicated the

axial stiffness of the cell. The rigid glass pipette onto

which the ®bre was attached was moved along the

longitudinal axis of the cell (Xm), as controlled by a

hydraulic micromanipulator (Narashige). At the same

time, the amount of reduction in cell length (Xc) due to

the compression was recorded on tape and the process

was played back for measurement of Xc using the frame

grabber and analysis software. An example of the

results obtained from an axial stiffness measurement is

illustrated in Figure 1(b), where a cell was compressed

by a quartz ®bre with a bending stiffness of

0.25 mN m)1. The ®bre was moved along the longi-

tudinal axis from 0.5 to 3 lm (Xm) in steps of 0.5 lm,

causing a decrease in cell length of 0.11±0.56 lm. The

force (F) exerted on the cell was equal to the amount of

bending of the ®bre (Xm ) Xc) multiplied by the

bending stiffness (d) of the ®bre. The force was plotted

against the compression-induced change in cell length,

with the slope of the linear regression line as the axial

stiffness of the cell. In this case, the calculated axial

stiffness of the cell was 0.63 mN m)1.

Shape changes in isolated outer hair cells

Hypertonic medium was prepared by adding 20±40 mM

sucrose to the culture medium, producing an �5±9%

rise in osmolality as measured by freezing point de-

pression (Roebling). Hypotonic medium was obtained

Outer hair cell stiffness � E Chan and M Ulfendahl Acta Physiol Scand 1997, 161, 533±539

534 Ó 1997 Scandinavian Physiological Society

by adding distilled water to the culture medium (5±10%

dilution), resulting in an �5±11% reduction in osmol-

ality. Exchange of the normal culture medium with the

hyper- or hypotonic media was achieved by perfusion at

a rate of 50±300 lL min)1 using a peristaltic pump

(Ismatec MS Reglo). In order to maintain the health state

of the cell and allow suf®cient time for cellular adjust-

ments, a slower perfusion rate was used if a greater

change in the osmolality was to be expected. Individual

cells were exposed only once to a change in osmolality.

In the experimental study, the axial stiffnesses of

isolated outer hair cells before and 10±12 min after

exposure to hyper- and hypotonic media were measured.

For the control study, three repetitive stiffness mea-

surements were obtained from each chosen cell at a time

interval of 12 min, i.e. at 0, 12 and 24 min, while the

osmolality of the external medium remained unchanged.

Statistical analysis

The mean stiffness values obtained from both the

experimental and control studies were expressed as

mean � SEM and were analysed using the non-para-

metric Wilcoxon matched-pairs signed-rank test. In

situations when a deterioration in the state of the cells

was observed during the exposure to the osmotically

modi®ed external medium, the measured stiffness val-

ues were also excluded from the statistical analysis.

RESULTS

Stiffness of outer hair cells

Axial stiffness was obtained from isolated outer hair

cells of body length ranging from 32 to 87 lm. Longer

cells seemed to survive the dissociation procedure

better than shorter cells and a greater number of long

cells with healthy appearance were found. This resulted

in a larger number of stiffness measurements made

from longer cells. As indicated by the linear regression

line, there is an inverse relationship between the cell

length and axial stiffness (Fig. 2a), i.e. longer cells are

found to be less stiff than shorter cells. The mean

stiffness of the long cells (³ 60 lm) was 1.05 �

0.12 mN m)1 �n � 34�, which was about 50% of

that obtained from the short cells (< 60 lm) of

2.21 � 0.67 mN m)1 �n � 6�.

Figure 1 (a) Diagramatic illustration of a quartz ®bre (QF) with one end ®xed to a glass pipette and the other end loaded with glass beads (B) of

different weights causing bending of the ®bre. The bending stiffness (d) is represented by the equation: F � dd, where F is the amount of force

exerted by the glass beads, and d is the amount of the bending displacement of the ®bre tip. As an example, the values for F and d were measured

from a quartz ®bre and were plotted as the graph shown. The slope of the curve is the bending stiffness (d), which was calculated to be

0.25 mN m)1 for this particular quartz ®bre of length 1.24 mm and diameter 2.78 lm. (b) The same quartz ®bre was placed adjacent to an

isolated outer hair cell (OHC), and the ®bre was moved a horizontal distance of (Xm) and the compression-induced cell length reduction of the

cell was Xc. The amount of the force (F) exerted onto the cell was calculated from the equation F = (Xm ± Xc)d, where d for this particular

quartz ®bre was 0.25 mN m)1. A graph of F against Xc was plotted and the slope of the curve represents the axial stiffness of the cell, which was

0.63 mN m)1 for this particular cell with a cell length of 86.60 lm and a diameter of 9.70 lm. N, nucleus; CP, cuticular plate.


Acta Physiol Scand 1997, 161, 533±539 E Chan and M Ulfendahl � Outer hair cell stiffness

The cell stiffness values were divided into two

groups according to the sites where the measurements

were made; they were either at the tip of the cuticular

plate or at its opposite side (inset, Fig. 2b). Among the

total population of stiffness measurements made, 19

cells were measured at the tip of the cuticular plate and

21 cells were measured at the other side. The results

showed that measuring from the two locations of the

cuticular plate did not produce a signi®cant difference

in the mean stiffness values (Fig. 2b).

The cell length and axial stiffness of the outer hair cells

were plotted against the cell diameter, and the data

points were extrapolated with linear regression lines

(Fig. 3). The trends of the lines indicated two opposite

relationships ± the cell diameter was inversely related to

the cell length but was directly related to the cell stiff-

ness.

Changes in tonicity and axial stiffness

When cells were exposed to hypertonic medium, they

became elongated and there was a decrease in cell

diameter. The resulting shape changes were often in the

range of a few percentage points and could only be

detected using the more sensitive image analysis tools.

Figure 4(a) shows a typical observation from a cell

before and after exposure to a hypertonic medium

producing a 9.7% increase in osmolality. The 2.0%

increase in cell length and 3.0% decrease in cell diam-

eter were accompanied by a 44.8% decrease in cell

stiffness. Figure 4(b) shows the changes observed from

another cell that was exposed to a hypotonic medium

giving a 5.0% decrease in osmolality. The resulting

1.6% decrease in cell length and increase in cell diam-

eter were accompanied by a 35.9% increase in cell

stiffness.

Figure 5 shows that exposure to a 7.51 � 0.62%

�n � 8� increase in osmolality (hypertonic) caused a

signi®cant decrease �P � 0:0391� in cell stiffness from

1.95 � 0.51 to 0.93 � 0.14 mN m)1 �n � 8�, corre-

sponding to a 48% change. On the other hand, expo-

sure to a 6.21 � 0.83% �n � 7� reduction in osmolality

(hypotonic) caused a 71% increase in cell stiffness,

from 0.87 � 0.12 to 1.49 � 0.40 mN m)1 (n � 7;

P � 0:0313). Approximately one-half of the cells

showed a recovery in the stiffness following washout of

the hyper- or hypotonic media. Control study from cells

�n � 11� that were kept at constant osmolality showed

no signi®cant change �P > 0:5� in stiffness over a

24 min period.

The changes in cell length and diameter in response to

the change in osmolality were also measured. The

Figure 2 (a) Axial stiffness of isolated

outer hair cells plotted against the cell

length. The mean of the 40 data points is

1.23 � 0.15 mN m)1. The regression line

is given by Sax � 4:61ÿ 0:048 L, where

Sax is the axial stiffness and L is the length

of the cell (correlation coef®cient, )0.67).

(b) Axial stiffness obtained from two

locations of the cuticular plate (see inset),

the tip �n � 19� and the opposite side of

the tip �n � 21�, was plotted against the

cell length.

Figure 3 Cell length (j) and axial stiffness (u) plotted against cell

diameter of isolated outer hair cells �n � 40�, and the corresponding

linear ®ts. Mean cell diameter was 9.69 � 0.14 lm �n � 40�.



results showed that exposure to hypertonic medium led

to a 3.52 � 1.41% increase in cell length and a

5.28 � 1.55% decrease in cell diameter �n � 8�; on the

other hand, exposure to hypotonic medium led to a

4.95 � 1.17% decrease in cell length and a

5.10 � 1.41% increase in cell diameter �n � 7�. The

effect of the change in osmolality to cell volume was

also estimated by assuming that the shape of the outer

hair cells resembles that of a cylinder. The calculations

have shown a decrease in cell volume in hypertonic

conditions and an increase in cell volume in hypotonic

conditions.

DISCUSSION

Cell length and diameter are related to axial stiffness

We measured the axial stiffness of isolated outer hair

cells, and attempted to relate it to cell length and

diameter. The principle for the measurement of

stiffness was similar to that used by others (Holley &

Ashmore 1988, Howard & Hudspeth 1988, Hallworth

1995) but with slightly modi®ed methods. The axial

stiffness values that we have obtained from the cells are

within the same range (0.15±25 mN m)1) as reported

elsewhere (Holley & Ashmore 1988, Hallworth 1995,

Russell & Schauz 1995). This suggests that the different

methods of measurement do not cause large discrep-

ancy in the stiffness values. The axial stiffness was

found to be inversely related to the cell length. The

observation was again in agreement with most of the

other studies (e.g. Hallworth 1995, Russell & Schauz

1995) but contrasted with that by Tolomeo et al. (1996).

The fact that there was an equal stiffness regardless of

where the measurement was made in relation to the

cuticular plate suggests that the force needed to bend

the cuticular plate is not related to the structural

polarization of the cells. Although a large variation was

seen from the plots of cell length and axial stiffness vs.

cell diameter, the linear regression lines indicate that the

longer and thinner the cells, the less stiff they are.

Minor change in cell shape in modi®ed tonic conditions

can result in signi®cant change in axial stiffness

Exposure to changes in tonicity causes a change in cell

shape, and the majority (>80%) of the observed changes

were similar to that reported by Chertoff & Brownell

(1994), i.e. cells become longer and thinner upon expo-

sure to hypertonic medium, and the opposite was ob-

Figure 4 (a) An isolated outer hair cell

before and after exposure to a 9.40%

increase in the osmolality of the external

medium (hypertonic). The cell length

increased from 77.49 to 79.00 lm, and the

cell diameter decreased from 8.71 to

8.43 lm. The axial stiffness of the cell

decreased from 1.11 to 0.61 mN m)1.

(b) An isolated outer hair cell before and

after exposure to a 5.00% decrease in the

osmolality of the external medium

(hypotonic). The cell length decreased

from 91.50 to 90.00 lm, and the cell

diameter increased from 9.37 to 9.52 lm.

The axial stiffness of the cell increased

from 0.81 to 1.10 mN m)1.

Figure 5 Mean axial stiffness values of cells before exposure to

hyper- and hypotonic media were compared with those after the

exposures. The axial stiffness was signi®cantly reduced �P � 0:0391,

n � 8) from 1.95 � 0.51 to 0.93 � 0.14 mN m)1 after exposure to

the hypertonic medium with a 7.46 � 0.54% increase in osmolality.

After exposure to the hypotonic medium with a 6.21 � 0.83%

decrease in osmolality, the axial stiffness was increased signi®cantly

(P � 0:0313, n � 7) from 0.87 � 0.12 to 1.49 � 0.40 mN m)1.



served upon exposure to hypotonic medium. In hypo-

tonic conditions, in¯ux of water causes an increase in cell

volume. The subsequent increase in internal cell pressure

leads to extension of the lateral cell membrane in the

transverse direction. The increased tension in the cell

membrane produces a pulling force along the cell axis,

resulting in cell shortening. The opposite occurs in

hypertonic conditions, where ef¯ux of water and

reduction of cell volume cause the lateral cell

membrane to relax in the longitudinal direction, leading

to an increase in cell length and a decrease in cell diam-

eter. Hence, the way that the cells changed their shape in

conditions of modi®ed external tonicity supports the

notion of a spring-like elastic component located along

the lateral cell membrane (Holley & Ashmore 1988). In

addition, the way that the cells were able to maintain a

cylindrical shape rather than becoming spherical when

encountered with hypotonic conditions suggests that the

cytoskeletal proteins can resist chronic changes in cell

shape due to external factors.

We have observed a volume regulation behaviour

from over 90% of the cells during exposure to a change

in tonicity, and the phenomenon was similar to that

reported by Crist et al. (1993). Cells changed their shape

upon initial exposure but returned partially to their

original shape after having been exposed to the

modi®ed osmotic environment for about 5 min. This

suggests that isolated outer hair cells are capable of

self-adjusting their shape in certain conditions.

The amount of shape change due to external factors

seems to be relatively less dramatic than the accom-

panied change in the cell stiffness. A change of less

than 10% in the cell diameter and cell length in hyper-

or hypotonic conditions led to an average 60% change

in the cell stiffness. Thus, as the results imply, when the

mechanical properties of isolated cells are measured,

cells having the same length and diameter may have

very different cell stiffnesses, depending on the internal

pressure condition of the cells. The observation may

also explain the scatter in cell stiffness obtained from

the otherwise normal-looking cells.

Cell shape and axial stiffness vs. time

Interestingly, it was demonstrated from the control

study that the time factor can change the relationship

between the cell shape and cell stiffness of individual

outer hair cells. It was found that by keeping the

tonicity of the external medium unchanged, there was a

time-dependent decrease in cell length over a period of

24 min, while there was no signi®cant change in cell

stiffness. Thus, the time-dependent cell length reduc-

tion was not accompanied by an increase in cell stiff-

ness, which is in contrast to that in modi®ed tonic

conditions when the change in cell shape resulted in a

change in cell stiffness. The observation here may be

explained by two concurrent factors: ®rstly, the change

in cell shape was an indication of deterioration of the

cell membrane over time, leading to an in¯ux of water;

and secondly, the condition of the cytoskeletal proteins

had also been changed. Here the two factors might

have led to opposite effects on the cell stiffness, with

the in¯ux of water causing an increase in stiffness and

the change in the condition of the cytoskeletal proteins

causing a decrease in stiffness. Thus, the two opposite

changes had cancelled out each other and resulted in

little change in total cell stiffness. The actual effect of a

change in the condition of the cytoskeletal proteins on

cell stiffness would, however, need further investiga-

tion.

The present results have demonstrated that the shape,

internal cell pressure and cell stiffness of the isolated

outer hair cells are related to each other. In addition,

the internal cell pressure seems to contribute signi®-

cantly to the stiffness of the outer hair cells. Hence, the

conditions of the internal cell pressure and the cyto-

skeletal network alone can probably re¯ect most of the

stiffness property of an outer hair cell.

This research was supported by grants from the Swedish Council for

Work Life Research (94±0151, 96±0715), the Swedish Medical

Research Council (09888), Stiftelsen Tysta Skolan, the Swedish

Institute and Stiftelsen Ragnhild och Einar LundstroÈms Minne.

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Documents

Relationship between stiffness, internal cell pressure and shape of outer hair cells isolated from the guinea-pig hearing organ